Elsevier

Cortex

Volume 126, May 2020, Pages 16-25
Cortex

Research Report
Reward presentation reduces on-task fatigue in traumatic brain injury

https://doi.org/10.1016/j.cortex.2020.01.003Get rights and content

Abstract

While cognitive fatigue is experienced by up to 80% of individuals with traumatic brain injury (TBI), little is known about its neural underpinnings. We previously hypothesized that presentation of rewarding outcomes leads to cognitive fatigue reduction and activation of the striatum, a brain region shown to be associated with cognitive fatigue in clinical populations and processing of rewarding outcomes. We have demonstrated this in individuals with multiple sclerosis. Here, we tested this hypothesis in individuals with TBI. Twenty-one individuals with TBI and 24 healthy participants underwent functional magnetic resonance imaging. Participants performed a task during which they were presented with 1) the Outcome condition where they were exposed to monetary rewards, and 2) the No Outcome condition that served as the control condition and was not associated with monetary rewards. In accordance with our hypothesis, results showed that attainment of rewarding outcomes leads to cognitive fatigue reduction in individuals with TBI, as well as activation of the striatum. Specifically, we observed a significant group by condition interaction on fatigue scores driven by the TBI group reporting lower levels of fatigue after the Outcome condition. fMRI data revealed a significant main-effect of condition in regions previously implicated in outcome processing, while a significant group by condition interaction was observed in the left ventral striatum as revealed by a priori region of interest analysis. Results suggest that a salient motivator can significantly reduce fatigue and that outcome presentation leads to increased activation of the ventral striatum in TBI. These findings can inform the development of future non-pharmacological cognitive fatigue treatment methods and contribute to the growing body of evidence showing the association between cognitive fatigue and the striatum.

Introduction

Fatigue is a common symptom in several clinical populations (Dobryakova, DeLuca, Genova, & Wylie, 2013) including multiple sclerosis (MS) (Dobryakova et al., 2015), Parkinson's disease (PD) (Friedman et al., 2011, Siciliano et al., 2018), stroke (Ingles et al., 1999), cancer (Barsevick, Frost, Zwinderman, Hall, & Halyard, 2010), and chronic fatigue syndrome (Cook, O’Connor, Lange, & Steffener, 2007). Fatigue is a multi-dimensional phenomenon, and while physical fatigue has been clearly defined (inability to sustain physical force or activity) and measured (e.g., with force measurement or electromyography), this has not been the case with cognitive fatigue. According to a seminal review by Chaudhuri and Behan (2004) cognitive fatigue can be defined as a subjective feeling of difficulty in initiating or sustaining voluntary mental tasks (Chaudhuri & Behan, 2004). It is usually assessed via a self-report questionnaire where participants answer questions about the degree to which fatigue influenced various activities that they performed during previous weeks. In individuals with traumatic brain injury (TBI), cognitive fatigue is reported to be experienced by up to 80% of affected individuals (Cantor, Gordon, & Gumber, 2013). Cognitive fatigue in TBI has been reported to be associated with reduced quality of life (Cantor et al., 2013) and negative rehabilitation outcomes (Zgaljardic et al., 2014). Despite its prevalence and impact, little is known about the neural underpinnings of cognitive fatigue. Such knowledge can inform how fatigue can be managed and treated in individuals with TBI.

Recent neuroimaging evidence implicates the striatum in cognitive fatigue experienced by persons with MS (Damasceno et al., 2015, Pardini et al., 2010), stroke (Tang et al., 2010, Tang et al., 2013), and Parkinson's disease (Kluger et al., 2019), including individuals with TBI (Dobryakova et al., 2013, Dobryakova et al., 2015, Ryan et al., 2016). Specifically, structural neuroimaging studies on cognitive fatigue point to the involvement of the striatum in persons with MS (Damasceno et al., 2015, Pardini et al., 2010), TBI (Ryan et al., 2016), stroke (Tang et al., 2010, Tang et al., 2013), and Parkinson's disease (Kluger et al., 2019), with striatal lesions and reduced white matter integrity and volume being associated with increased levels of fatigue. The striatum is a subcortical structure that receives projections from dopamine neurons. It plays a pivotal role in motivation, learning, and processing of rewarding and punishing outcomes during goal-attainment (Tricomi et al., 2017). Specifically, animal studies show that unexpected outcome presentation during motivated behavior is associated with increased firing rate of dopamine neurons and cessation of neuronal firing during outcome omission. fMRI studies provide convergent evidence in healthy individuals (Delgado et al., 2000, Dobryakova et al., 2017, Dobryakova and Tricomi, 2013), while positron emission tomography studies in healthy individuals indicate that there is dopamine release during presentation of rewarding outcomes.e.g., (Pappata et al., 2002, Weiland et al., 2014)

It is this involvement in motivation and processing of rewarding and punishing outcomes during goal-attainment that is called upon to explain the role of the striatum in fatigue. A preponderance of evidence indicates that dysfunction of the striatum leads to deficits in the processing of rewarding outcomes in clinical populations (Griffiths et al., 2014). Such deficits can lead to the experience of fatigue in affected individuals (Dobryakova et al., 2015, Müller and Apps, 2018). However, striatal dysfunction in conjunction with rewarding outcome processing has not been examined in individuals with TBI. We have previously hypothesized that engaging in behaviors that are motivated by the presentation of rewarding outcomes would lead to cognitive fatigue reduction through the engagement of the striatum and have demonstrated that presentation of rewarding outcomes leads to both cognitive fatigue reduction and increased activation of the striatum in individuals with MS (Dobryakova et al., 2018). In the current study, we tested the hypothesis that the striatum plays a critical role in cognitive fatigue reduction in individuals with TBI. Specifically, we examined whether cognitive fatigue experienced during task performance (on-task fatigue that is experienced in the moment) can be reduced through the presentation of monetary rewards and whether reward presentation elicits increased activation in the striatum in individuals with TBI as compared to healthy controls (HCs). Money is a salient motivator and thus drives a variety of human behaviors. We thus hypothesized that TBI participants will report less fatigue when they perform a task where they are motivated by obtaining monetary rewards and will report higher levels of fatigue when the motivation to obtain monetary rewards is absent. Since assessment of the brain activity is related to a specific task, we measured on-task fatigue that is related to the same time period as task performance and is tied to that time period.

Section snippets

Participants

To qualify for the study, participants with TBI had to get an average score 4 or above on the Fatigue Severity Scale (FSS) (Flachenecker et al., 2002, Krupp et al., 1989). Given that fatigue was the symptom of interest, we did not exclude based on TBI severity. Twenty-one individuals with mild-to-severe TBI and 24 HCs participated in the study (see Table 1). Participants were recruited through advertisements and word of mouth, through the Northern New Jersey TBI Model System and/or through the

VAS-F scores

In accordance with our hypothesis, 2 (group) x 2 (condition) ANOVA on VAS-F scores revealed a significant group by condition interaction (F(1,43) = 4.67, p < .04, η2 = .1,1 medium effect size; Fig. 2), demonstrating that attainment of rewarding outcomes resulted

Discussion

The current study examined a novel approach to cognitive fatigue reduction in TBI. While cognitive fatigue can be affected by many factors, in the current study we examined the impact of rewarding outcome presentation on cognitive fatigue, while minimizing effects such as learning and effort. Specifically, we showed that cognitive fatigue in individuals with TBI can be reduced through the presentation of rewarding outcomes. These results suggest that a salient motivator (such as money in the

Conclusions

In the current investigation, we showed that reward presentation leads to on-task fatigue reduction and striatal activation in individuals with TBI. The current findings suggest that utilization of behavioral strategies, such as reward presentation, might lead to fatigue reduction by activating brain regions engaged in these strategies. In addition, the current study extends findings from healthy populations (Boksem, Meijman, & Lorist, 2006) and individuals with MS (Dobryakova et al., 2018) to

Open practices

The study in this article earned Open Materials and Open Data badges for transparent practices. Materials and data for the study are available at https://osf.io/4pvbm/?view_only=f65d7c3c43fc4e5e8ac5d66151ed539e.

CRediT authorship contribution statement

Ekaterina Dobryakova: Conceptualization, Writing - original draft, Formal analysis, Funding acquisition. Helen Genova: Conceptualization. Veronica Schneider: Formal analysis. Nancy D. Chiaravalloti: Writing - review & editing. Angela Spirou: Formal analysis. Glenn R. Wylie: Writing - review & editing. John DeLuca: Conceptualization.

Declaration of Competing Interest

No competing financial interests exist.

Acknowledgement

This work was supported by the National Institute for Independent Living, Disability and Rehabilitation (Award#90SF00090100), awarded to Ekaterina Dobryakova, PhD.

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